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Parasitic Castration by the Digenian Trematode Allopodocotyle Sp. Alters Gene Expression in the Brain of the Host Mollusc Haliotis Asinina

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Parasitic Castration by the Digenian Trematode Allopodocotyle Sp. Alters Gene Expression in the Brain of the Host Mollusc Haliotis Asinina View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector FEBS Letters 580 (2006) 3769–3774 Parasitic castration by the digenian trematode Allopodocotyle sp. alters gene expression in the brain of the host mollusc Haliotis asinina Tamika Ricea, Elizabeth McGrawa, Elizabeth K. O’Briena, Antonio Reverterb, Daniel J. Jacksona, Bernard M. Degnana,* a School of Integrative Biology, University of Queensland, Brisbane, Qld. 4072, Australia b CSIRO Livestock Industries, Brisbane, Qld. 4067, Australia Received 22 March 2006; revised 16 May 2006; accepted 25 May 2006 Available online 9 June 2006 Edited by Takashi Gojobori schistosome trematode, Trichobilharzia ocellata [7,10,11], cas- Abstract Infection of molluscs by digenean trematode parasites typically results in the repression of reproduction – the so-called tration appears to be caused by induced changes in gene parasitic castration. This is known to occur by altering the expression of the neuroendocrine system that controls growth expression of a range of host neuropeptide genes. Here we ana- and reproduction [2]. lyse the expression levels of 10 members of POU, Pax, Sox and The neurosecretory system of molluscs consists primarily of Hox transcription factor gene families, along with genes encod- individual or small clusters of neurons distributed throughout ing FMRFamide, prohormone convertase and b-tubulin, in the the cerebral, pleural, pedal and visceral ganglia [12]. The brain ganglia of actively reproducing (summer), non-reproducing antagonism between growth and reproduction appears to be (winter) and infected Haliotis asinina (a vetigastropod mollusc). controlled by neurohormones synthesised by cells in these gan- A number of the regulatory genes are differentially expressed in glia [13]. Physiological changes occurring in both normal and parasitised H. asinina, but in only a few cases do expression pat- infected L. stagnalis correlate with changes in expression of terns in infected animals match those occurring in animals where reproduction is normally repressed. genes encoding neuropeptides, such as: (i) schistosomin, which Ó 2006 Published by Elsevier B.V. on behalf of the Federation of inhibits the action of gonadotropic hormones in reproductive European Biochemical Societies. organs; (ii) neuropeptide Y, which appears to regulate repro- duction and growth; and (iii) caudodorsal cell hormone, which Keywords: Digenean; Hox; Pax; POU; Transcription factor; is known to regulate egg-laying and accompanying behaviours Sox; Haliotis [2]. The activities of specific cell clusters in the ganglia with known roles in reproduction and growth are also affected by parasitosis [7,14,15]. Regulatory transcription factors are likely to act as key controllers in the normal physiological transi- 1. Introduction tions operating in molluscan ganglia [16], and coordinate the expression of gene batteries that are required for the mollusc Digenean trematodes are platyhelminth parasites with com- to obtain a reproductive or growing physiological state. plex lifecycles, typically involving at least three different hosts Haliotis asinina (Vetigastropoda) has a distinct and predict- including a definitive, a first intermediate and a second inter- able reproductive season that lasts for about six months in the mediate host [1]. The first intermediate host is almost always summer [17]. During this season the ovaries are full of mature a mollusc, with a given digenean species capable of infecting oocytes, while during the non-reproductive winter period, the only one or two mollusc species [1]. These strict associations female gonad consists of small numbers of immature oocytes have allowed specialised interactions to evolve, including par- and granular debris [26]. Approximately 2% of wild population asite-induced alterations in host behaviour, defence function, of H. asinina of Heron Island Reef are infected with an opeco- nutrition, metabolism and reproduction [2–4]. One common elid digenean in the genus Allopodocotyle [8]. The condition of outcome of digenean infection in molluscs is castration [5–8], the gonads of these parasitised abalone imitates that of the which can result in the incomplete or total disruption of host non-gravid winter gonads, with no direct structural damage gamete production and presumably allow for the redeploy- observed. In infected abalone, the sporocyst and cercarial ment of metabolites to the parasite [9]. stages inhabit the haemocoel suggesting that parasitic castra- In most cases castration occurs indirectly, either through the tion is likely to be because of effects to the physiology of the deprivation of essential nutrients [6] or by the interruption and host and not direct consumption of the gonad by the trema- utilisation of the host’s natural endocrine system [7,10,11].In tode. Infections of other host molluscs largely appear to follow the interaction between the snail, Lymnaea stagnalis, and the similar patterns of castration [5–7]. In this study, we have quantitatively assessed the expression of 10 transcription fac- tor genes, along with FMRFamide, prohormone convertase *Corresponding author. Fax: +61 7 3365 1655. 2 (PC2), and tubulin genes in the cerebral and pleuropedal E-mail address: [email protected] (B.M. Degnan). ganglia of H. asinina that are either: (i) actively reproducing; (ii) parasitized and castrated; and (iii) not reproducing. The Abbreviations: ANOVA, one-way analysis of variances; PC2, prohor- mone convertase 2; QPCR, quantitative real-time reverse transcription transcription factor families targeted for quantification – polymerase chain reaction Hox, Pax, POU and Sox – are known to play key roles in 0014-5793/$32.00 Ó 2006 Published by Elsevier B.V. on behalf of the Federation of European Biochemical Societies. doi:10.1016/j.febslet.2006.05.068 3770 T. Rice et al. / FEBS Letters 580 (2006) 3769–3774 development of a wide range of animals and in some cases mer abalone), when not reproducing (winter abalone) or when physiological processes such as growth [18,19]. These genes infected by the digenean trematode (parasitised). The infected are expressed in tissue-restricted patterns in H. asinina and in animals were all obtained in the summer, when they normally brain ganglia [16,20–23]. would be reproducing. 3.1. Expression of reference gene HasSox-C 2. Materials and methods HasSox-Cwas chosen as the reference gene as it is widely ex- pressed during development and across adult tissues [16,20,21]. 2.1. Collection of samples However, QPCR revealed that the HasSox-C expression levels H. asinina were collected on Heron Island Reef Australia. Parasi- in the cerebral ganglia were 1.7-fold different between winter tised abalone were identified by inspecting the gonad region for obvi- and summer samples (Fig. 1). Expression levels in the pleuro- ous infestation of sporocysts as per [8]. Total RNA was extracted from individual dissected cerebral and pleuropedal ganglia from reproduc- pedal ganglia were higher and more variable, with winter sam- ing (summer) abalone, non-reproductive (winter) abalone or parasi- ples having the highest level of expression and parasitised tised summer abalone as described in [16]. samples showing a significantly lower transcript levels than either of the uninfected treatments. HasSox-C was employed 2.2. Quantitative real-time PCR as a reference despite the uneven expression across seasons cDNA was synthesised using 0.2 lg of RNA, 10 lM random hexa- and between normal and parasitised animals. The effect of mer primers (Promega) and MMLV-reverse transcriptase (Promega) these differences in HasSox-C transcript abundance, however, according to the manufacturer’s specifications. Gradient polymerase chain reactions (PCRs) were performed on all primer sets (oligonucleo- was mitigated by defining a set of correction factors for each tide primer sequences available upon request) to ascertain a uniformly ganglia. Expression in each of the parasitised ganglia was set suitable annealing temperature, using 0.01 lg cDNA per 20 ll reac- to 1 and the fold difference between parasitised and the other tion. The cycling conditions for all gradient PCRs were 96 °C for samples was calculated. The correction factors were as follows: 2 min, 35 cycles of 94 °C for 30 s, gradient annealing from 53 to cerebral ganglia summer = 0.78 and winter = 1.34; and pleuro- 68 °C for 1 min, 72 °C for 1 min followed by a final extension of 72 °C for 10 min and a cooling to 25 °C for 10 min. pedal ganglia summer = 2.79 and winter = 4.25 (Fig. 1; Table Quantitative real-time reverse transcription polymerase chain reac- 1). These correction factors were applied to the normalised tion (QPCR) was conducted on a LightCycler (Roche) using Quanti- abundance values to produce the standardised abundance tech SYBR Green PCR Mix (Qiagen). The master mix was values. optimised to contain 0.75· SYBR Green Mix, 1 lM per primer, and 0.01 lg cDNA per 20 ll reaction. cDNA samples made from differing amounts of initial RNA (0.2 lg, 0.4 lg, 0.6 lg and 1 lg) were run as 3.2. Structural and neuropeptide gene expression profiles standards in each run. Standards were run in triplicate and each sam- Overall, HasTub1, HasPC2, and HasFMRFa transcripts ple in triplicate for the control gene and the gene of interest. All runs were more abundant in both ganglia compared to transcripts included a negative control. For all analyses the cycling conditions were 95 °C for 15 min, 32 cycles of 94 °C for 30 s, 56 °C for 1 min, encoding transcription factors (Fig. 2). HasTub1 and HasPC2 72 °C for 1 min with a read temperature of 80 °C each cycle. Melting were expressed at higher levels in the ganglia of non-reproduc- curve analysis was used to establish that only one product was ampli- ing animals in the winter, with 2.4-fold higher expression of fied per reaction and that the product was the expected amplicon. HasTub1 in the cerebral ganglion and approximately 20-fold higher expression of HasPC2 in both ganglia (Table 1).
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